Advertisement

Chromosome Research

, Volume 27, Issue 3, pp 153–165 | Cite as

Fluorescence in situ hybridization in plants: recent developments and future applications

  • Jiming JiangEmail author
Waldeyer-Flemming Special Collection

Abstract

Fluorescence in situ hybridization (FISH) was developed more than 30 years ago and has been the most paradigm-changing technique in cytogenetic research. FISH has been used to answer questions related to structure, mutation, and evolution of not only individual chromosomes but also entire genomes. FISH has served as an important tool for chromosome identification in many plant species. This review intends to summarize and discuss key technical development and applications of FISH in plants since 2006. The most significant recent advance of FISH is the development and application of probes based on synthetic oligonucleotides (oligos). Oligos specific to a repetitive DNA sequence, to a specific chromosomal region, or to an entire chromosome can be computationally identified, synthesized in parallel, and fluorescently labeled. Oligo probes designed from conserved DNA sequences from one species can be used among genetically related species, allowing comparative cytogenetic mapping of these species. The advances with synthetic oligo probes will significantly expand the applications of FISH especially in non-model plant species. Recent achievements and future applications of FISH and oligo-FISH are discussed.

Keywords

FISH Oligo-FISH Karyotype Chromosome Genome Evolution 

Abbreviations

BAC

Bacterial artificial chromosome

ChIP

Chromatin immunoprecipitation

eccDNA

Extrachromosomal circular DNA

FISH

Fluorescence in situ hybridization

Mys

Million years

Oligo

Oligonucleotide

SSR

Simple-sequence repeats

Notes

Acknowledgments

FISH images in Fig. 2 were developed by Guilherme Braz, Li He, Tao Zhang, and Pingdong Zhang.

Funding information

Cytogenetic research in the author’s lab has been supported by National Science Foundation (NSF) grants IOS-1444514 and MCB-1412948.

References

  1. Albert PS, Zhang T, Semrau K, Rouillard J-M, Kao Y-H, Wang C-JR, Danilova TV, Jiang JM, Birchler JA (2019) Whole-chromosome paints in maize reveal rearrangements, nuclear domains, and chromosomal relationships. Proc Natl Acad Sci U S A 116:1679–1685Google Scholar
  2. Aliyeva-Schnorr L, Beier S, Karafiatova M, Schmutzer T, Scholz U, Dolezel J, Stein N, Houben A (2015a) Cytogenetic mapping with centromeric bacterial artificial chromosomes contigs shows that this recombination-poor region comprises more than half of barley chromosome 3H. Plant J 84:385–394Google Scholar
  3. Aliyeva-Schnorr L, Ma L, Houben A (2015b) A fast air-dry dropping chromosome preparation method suitable for FISH in plants. J Vis Exp:e53470Google Scholar
  4. Aliyeva-Schnorr L, Stein N, Houben A (2016) Collinearity of homoeologous group 3 chromosomes in the genus Hordeum and Secale cereale as revealed by 3H-derived FISH analysis. Chromosom Res 24:231–242Google Scholar
  5. Amosova AV, Bolsheva NL, Samatadze TE, Twardovska MO, Zoshchuk SA, Andreev IO, Badaeva ED, Kunakh VA, Muravenko OV (2015) Molecular cytogenetic analysis of Deschampsia antarctica Desv. (Poaceae), maritime antarctic. Plos One 10:e0138878Google Scholar
  6. Beliveau BJ, Joyce EF, Apostolopoulos N, Yilmaz F, Fonseka CY, McCole RB, Chang YM, Li JB, Senaratne TN, Williams BR, Rouillard JM, Wu CT (2012) Versatile design and synthesis platform for visualizing genomes with Oligopaint FISH probes. Proc Natl Acad Sci U S A 109:21301–21306Google Scholar
  7. Belyayev A, Pastova L, Fehrer J, Josefiova J, Chrtek J, Mraz P (2018) Mapping of Hieracium (Asteraceae) chromosomes with genus-specific satDNA elements derived from next-generation sequencing data. Plant Syst Evol 304:387–396Google Scholar
  8. Betekhtin A, Jenkins G, Hasterok R (2014) Reconstructing the evolution of Brachypodium genomes using comparative chromosome painting. PLoS One 9:e115108Google Scholar
  9. Boyle S, Rodesch MJ, Halvensleben HA, Jeddeloh JA, Bickmore WA (2011) Fluorescence in situ hybridization with high-complexity repeat-free oligonucleotide probes generated by massively parallel synthesis. Chromosom Res 19:901–909Google Scholar
  10. Braz GT, He L, Zhao H, Zhang T, Semrau K, Rouillard JM, Torres GA, Jiang JM (2018) Comparative oligo-FISH mapping: an efficient and powerful methodology to reveal karyotypic and chromosomal evolution. Genetics 208:513–523Google Scholar
  11. Cabili MN, Dunagin MC, McClanahan PD, Biaesch A, Padovan-Merhar O, Regev A, Rinn JL, Raj A (2015) Localization and abundance analysis of human IncRNAs at single-cell and single-molecule resolution. Genome Biol 16:20Google Scholar
  12. Camacho JPM, Ruiz-Ruano FJ, Martin-Blazquez R, Lopez-Leon MD, Cabrero J, Lorite P, Cabral-de-Mello DC, Bakkali M (2015) A step to the gigantic genome of the desert locust: chromosome sizes and repeated DNAs. Chromosoma 124:263–275Google Scholar
  13. Carmona A, Friero E, de Bustos A, Jouve N, Cuadrado A (2013) Cytogenetic diversity of SSR motifs within and between Hordeum species carrying the H genome: H-vulgare L. and H-bulbosum L. Theor Appl Genet 126:949–961Google Scholar
  14. Cook DE, Lee TG, Guo XL, Melito S, Wang K, Bayless AM, Wang JP, Hughes TJ, Willis DK, Clemente TE, Diers BW, Jiang JM, Hudson ME, Bent AF (2012) Copy number variation of multiple genes at Rhg1 mediates nematode resistance in soybean. Science 338:1206–1209Google Scholar
  15. Cook DE, Bayless AM, Wang K, Guo XL, Song QJ, Jiang JM, Bent AF (2014) Distinct copy number, coding sequence, and locus methylation patterns underlie Rhg1-mediated soybean resistance to soybean cyst nematode. Plant Physiol 165:630–647Google Scholar
  16. Cuadrado A, Jouve N (2007) The nonrandom distribution of long clusters of all possible classes of trinucleotide repeats in barley chromosomes. Chromosom Res 15:711–720Google Scholar
  17. Cuadrado A, Schwarzacher T (1998) The chromosomal organization of simple sequence repeats in wheat and rye genomes. Chromosoma 107:587–594Google Scholar
  18. Dang JB, Zhao Q, Yang X, Chen Z, Xiang SQ, Liang GL (2015) A modified method for preparing meiotic chromosomes based on digesting pollen mother cells in suspension. Mol Cytogenet 8:80Google Scholar
  19. Danilova TV, Birchler JA (2008) Integrated cytogenetic map of mitotic metaphase chromosome 9 of maize: resolution, sensitivity, and banding paint development. Chromosoma 117:345–356Google Scholar
  20. Danilova TV, Friebe B, Gill BS (2012) Single-copy gene fluorescence in situ hybridization and genome analysis: Acc-2 loci mark evolutionary chromosomal rearrangements in wheat. Chromosoma 121:597–611Google Scholar
  21. Danilova TV, Friebe B, Gill BS (2014) Development of a wheat single gene FISH map for analyzing homoeologous relationship and chromosomal rearrangements within the Triticeae. Theor Appl Genet 127:715–730Google Scholar
  22. Danilova TV, Akhunova AR, Akhunov ED, Friebe B, Gill BS (2017) Major structural genomic alterations can be associated with hybrid speciation in Aegilops markgrafii (Triticeae). Plant J 92:317–330Google Scholar
  23. Deng WL, Shi XH, Tjian R, Lionnet T, Singer RH (2015) CASFISH: CRISPR/Cas9-mediated in situ labeling of genomic loci in fixed cells. Proc Natl Acad Sci U S A 112:11870–11875Google Scholar
  24. Dillon A, Varanasi VK, Danilova TV, Koo DH, Nakka S, Peterson DE, Tranel PJ, Friebe B, Gill BS, Jugulam M (2017) Physical mapping of amplified copies of the 5-enolpyruvylshikimate-3-phosphate synthase gene in glyphosate-resistant Amaranthus tuberculatus. Plant Physiol 173:1226–1234Google Scholar
  25. Dluhosova J, Istvanek J, Nedelnik J, Repkova J (2018) Red clover (Trifolium pratense) and zigzag clover (T. medium) - a picture of genomic similarities and differences. Front Plant Sci 9:724Google Scholar
  26. Doganlar S, Frary A, Daunay MC, Lester RN, Tanksley SD (2002) A comparative genetic linkage map of eggplant (Solanum melongena) and its implications for genome evolution in the Solanaceae. Genetics 161:1697–1711Google Scholar
  27. Dou QW, Chen ZG, Liu YA, Tsujimoto H (2009) High frequency of karyotype variation revealed by sequential FISH and GISH in plateau perennial grass forage Elymus nutans. Breed Sci 59:651–656Google Scholar
  28. Dreissig S, Schiml S, Schindele P, Weiss O, Rutten T, Schubert V, Gladilin E, Mette MF, Puchta H, Houben A (2017) Live-cell CRISPR imaging in plants reveals dynamic telomere movements. Plant J 91:565–573Google Scholar
  29. Duncan S, Olsson TSG, Hartley M, Dean C, Rosa S (2016) A method for detecting single mRNA molecules in Arabidopsis thaliana. Plant Methods 12:13Google Scholar
  30. Filiault DL, Ballerini ES, Mandáková T, Aköz G, Derieg NJ, Schmutz J, Jenkins J, Grimwood J, Shu S, Hayes RD, Hellsten U, Barry K, Yan J, Mihaltcheva S, Karafiátová M, Nizhynska V, Kramer EM, Lysak MA, Hodges SA, Nordborg M (2018) The Aquilegia genome provides insight into adaptive radiation and reveals an extraordinarily polymorphic chromosome with a unique history. eLife 7:e36426Google Scholar
  31. Fransz PF, Alonso-Blanco C, Liharska TB, Peeters AJM, Zabel P, de Jong JH (1996) High-resolution physical mapping in Arabidopsis thaliana and tomato by fluorescence in situ hybridization to extended DNA fibres. Plant J 9:421–430Google Scholar
  32. Fu SL, Chen L, Wang YY, Li M, Yang ZJ, Qiu L, Yan BJ, Ren ZL, Tang ZX (2015) Oligonucleotide probes for ND-FISH analysis to identify rye and wheat chromosomes. Sci Rep 5:10552Google Scholar
  33. Fuchs J, Strehl S, Brandes A, Schweizer D, Schubert I (1998) Molecular-cytogenetic characterization of the Vicia faba genome - heterochromatin differentiation, replication patterns and sequence localization. Chromosom Res 6:219–230Google Scholar
  34. Fujimoto S, Sugano SS, Kuwata K, Osakabe K, Matsunaga S (2016) Visualization of specific repetitive genomic sequences with fluorescent TALEs in Arabidopsis thaliana. J Exp Bot 67:6101–6110Google Scholar
  35. Gaiero P, van de Belt J, Vilaro F, Schranz ME, Speranza P, de Jong H (2017) Collinearity between potato (Solanum tuberosum L.) and wild relatives assessed by comparative cytogenetic mapping. Genome 60:228–240Google Scholar
  36. Gaines TA, Zhang WL, Wang DF, Bukun B, Chisholm ST, Shaner DL, Nissen SJ, Patzoldt WL, Tranel PJ, Culpepper AS, Grey TL, Webster TM, Vencill WK, Sammons RD, Jiang JM, Preston C, Leach JE, Westra P (2010) Gene amplification confers glyphosate resistance in Amaranthus palmeri. Proc Natl Acad Sci U S A 107:1029–1034Google Scholar
  37. Gong ZY, Wu YF, Koblizkova A, Torres GA, Wang K, Iovene M, Neumann P, Zhang WL, Novak P, Buell CR, Macas J, Jiang JM (2012) Repeatless and repeat-based centromeres in potato: implications for centromere evolution. Plant Cell 24:3559–3574Google Scholar
  38. Gortner G, Nenno M, Weising K, Zink D, Nagl W, Kahl G (1998) Chromosomal localization and distribution of simple sequence repeats and the Arabidopsis-type telomere sequence in the genome of Cicer arietinum L. Chromosom Res 6:97–104Google Scholar
  39. Han YH, Zhang ZH, Liu CX, Liu JH, Huang SW, Jiang JM, Jin WW (2009) Centromere repositioning in cucurbit species: implication of the genomic impact from centromere activation and inactivation. Proc Natl Acad Sci U S A 106:14937–14941Google Scholar
  40. Han YH, Zhang T, Thammapichai P, Weng YQ, Jiang JM (2015) Chromosome-specific painting in Cucumis species using bulked oligonucleotides. Genetics 200:771–779Google Scholar
  41. Han JL, Masonbrink RE, Shan WB, Song FQ, Zhang JS, Yu WC, Wang KB, Wu YF, Tang HB, Wendel JF, Wang K (2016) Rapid proliferation and nucleolar organizer targeting centromeric retrotransposons in cotton. Plant J 88:992–1005Google Scholar
  42. He QY, Cai ZX, Hu TH, Liu HJ, Bao CL, Mao WH, Jin WW (2015) Repetitive sequence analysis and karyotyping reveals centromere-associated DNA sequences in radish (Raphanus sativus L.). BMC Plant Biol 15:105Google Scholar
  43. He L, Braz GT, Torres GA, Jiang JM (2018) Chromosome painting in meiosis reveals pairing of specific chromosomes in polyploid Solanum species. Chromosoma 127:505–513Google Scholar
  44. Heitkam T, Petrasch S, Zakrzewski F, Kogler A, Wenke T, Wanke S, Schmidt T (2015) Next-generation sequencing reveals differentially amplified tandem repeats as a major genome component of Northern Europe’s oldest Camellia japonica. Chromosom Res 23:791–806Google Scholar
  45. Henikoff S, Ahmad K, Malik HS (2001) The centromere paradox: stable inheritance with rapidly evolving DNA. Science 293:1098–1102Google Scholar
  46. Hou LL, Xu M, Zhang T, Xu ZH, Wang WY, Zhang JX, Yu MM, Ji W, Zhu CW, Gong ZY, Gu MH, Jiang JM, Yu HX (2018) Chromosome painting and its applications in cultivated and wild rice. BMC Plant Biol 18:110Google Scholar
  47. Idziak D, Betekhtin A, Wolny E, Lesniewska K, Wright J, Febrer M, Bevan MW, Jenkins G, Hasterok R (2011) Painting the chromosomes of Brachypodium - current status and future prospects. Chromosoma 120:469–479Google Scholar
  48. Idziak D, Hazuka I, Poliwczak B, Wiszynska A, Wolny E, Hasterok R (2014) Insight into the karyotype evolution of Brachypodium species using comparative chromosome barcoding. PLoS One 9:e93503Google Scholar
  49. Iovene M, Wielgus SM, Simon PW, Buell CR, Jiang JM (2008) Chromatin structure and physical mapping of chromosome 6 of potato and comparative analyses with tomato. Genetics 180:1307–1317Google Scholar
  50. Iovene M, Cavagnaro PF, Senalik D, Buell CR, Jiang JM, Simon PW (2011) Comparative FISH mapping of Daucus species (Apiaceae family). Chromosom Res 19:493–506Google Scholar
  51. Iwata-Otsubo A, Lin JY, Gill N, Jackson SA (2016) Highly distinct chromosomal structures in cowpea (Vigna unguiculata), as revealed by molecular cytogenetic analysis. Chromosom Res 24:197–216Google Scholar
  52. Jackson SA, Wang ML, Goodman HM, Jiang JM (1998) Application of fiber-FISH in physical mapping of Arabidopsis thaliana. Genome 41:566–572Google Scholar
  53. Jackson SA, Dong FG, Jiang JM (1999) Digital mapping of bacterial artificial chromosomes by fluorescence in situ hybridization. Plant J 17:581–587Google Scholar
  54. Janda J, Safar J, Kubalakova M, Bartos J, Kovarova P, Suchankova P, Pateyron S, Cihalikova J, Sourdille P, Simkova H, Faivre-Rampant P, Hribova E, Bernard M, Lukaszewski A, Dolezel J, Chalhoub B (2006) Advanced resources for plant genomics: a BAC library specific for the short arm of wheat chromosome 1B. Plant J 47:977–986Google Scholar
  55. Jiang JM, Gill BS (1994) Nonisotopic in situ hybridization and plant genome mapping: the first 10 years. Genome 37:717–725Google Scholar
  56. Jiang JM, Gill BS (2006) Current status and the future of fluorescence in situ hybridization (FISH) in plant genome research. Genome 49:1057–1068Google Scholar
  57. Jiang JM, Birchler JA, Parrott WA, Dawe RK (2003) A molecular view of plant centromeres. Trends Plant Sci 8:570–575Google Scholar
  58. Jugulam M, Niehues K, Godar AS, Koo DH, Danilova T, Friebe B, Sehgal S, Varanasi VK, Wiersma A, Westra P, Stahlman PW, Gill BS (2014) Tandem amplification of a chromosomal segment harboring 5-enolpyruvylshikimate-3-phosphate synthase locus confers glyphosate resistance in Kochia scoparia. Plant Physiol 166:1200–1207Google Scholar
  59. Kato A, Albert PS, Vega JM, Birchler JA (2006) Sensitive fluorescence in situ hybridization signal detection in maize using directly labeled probes produced by high concentration DNA polymerase nick translation. Biotech Histochem 81:71–78Google Scholar
  60. Khrustaleva L, Jiang JM, Havey MJ (2016) High-resolution tyramide-FISH mapping of markers tightly linked to the male-fertility restoration (Ms) locus of onion. Theor Appl Genet 129:535–545Google Scholar
  61. Kirov I, Divashuk M, Van Laere K, Soloviev A, Khrustaleva L (2014a) An easy “SteamDrop” method for high quality plant chromosome preparation. Mol Cytogenet 7:21Google Scholar
  62. Kirov I, Van Laere K, De Riek J, De Keyser E, Van Roy N, Khrustaleva L (2014b) Anchoring linkage groups of the Rosa genetic map to physical chromosomes with Tyramide-FISH and EST-SNP markers. PLoS One 9:e95793Google Scholar
  63. Kirov IV, Kiseleva AV, Van Laere K, Van Roy N, Khrustaleva LI (2017) Tandem repeats of Allium fistulosum associated with major chromosomal landmarks. Mol Gen Genomics 292:453–464Google Scholar
  64. Kondrashov FA (2012) Gene duplication as a mechanism of genomic adaptation to a changing environment. Proc R Soc B Biol Sci 279:5048–5057Google Scholar
  65. Koo DH, Han FP, Birchler JA, Jiang JM (2011) Distinct DNA methylation patterns associated with active and inactive centromeres of the maize B chromosome. Genome Res 21:908–914Google Scholar
  66. Koo DH, Jugulam M, Putta K, Cuvaca IB, Peterson DE, Currie RS, Friebe B, Gill BS (2018a) Gene duplication and aneuploidy trigger rapid evolution of herbicide resistance in common waterhemp. Plant Physiol 176:1932–1938Google Scholar
  67. Koo DH, Molin WT, Saski CA, Jiang JM, Putta K, Jugulam M, Friebe B, Gill BS (2018b) Extrachromosomal circular DNA-based amplification and transmission of herbicide resistance in crop weed Amaranthus palmeri. Proc Natl Acad Sci U S A 115:3332–3337Google Scholar
  68. Kowar T, Zakrzewski F, Macas J, Koblizkova A, Viehoever P, Weisshaar B, Schmidt T (2016) Repeat composition of CenH3-chromatin and H3K9me2-marked heterochromatin in sugar beet (Beta vulgaris). BMC Plant Biol 16:120Google Scholar
  69. Kuo YT, Hsu HL, Yeh CH, Chang SB (2016) Application of a modified drop method for high-resolution pachytene chromosome spreads in two Phalaenopsis species. Mol Cytogenet 9:44Google Scholar
  70. Lamb JC, Danilova T, Bauer MJ, Meyer JM, Holland JJ, Jensen MD, Birchler JA (2007) Single-gene detection and karyotyping using small-target fluorescence in situ hybridization on maize somatic chromosomes. Genetics 175:1047–1058Google Scholar
  71. Lang T, Li G, Wang H, Yu Z, Chen Q, Yang E, Fu S, Tang Z, Yang Z (2018) Physical location of tandem repeats in the wheat genome and application for chromosome identification. Planta.  https://doi.org/10.1007/s00425-00018-03033-00424
  72. Langer-Safer PR, Levine M, Ward DC (1982) Immunological method for mapping genes on Drosophila polytene chromosomes. Proc Natl Acad Sci U S A Biol Sci 79:4381–4385Google Scholar
  73. Leitch IJ, Leitch AR, Heslopharrison JS (1991) Physical mapping of plant DNA sequences by simultaneous in situ hybridization of two differently labeled fluorescent probes. Genome 34:329–333Google Scholar
  74. Li YJ, Zuo S, Zhang ZL, Li ZJ, Han JL, Chu ZQ, Hasterok R, Wang K (2018a) Centromeric DNA characterization in the model grass Brachypodium distachyon provides insights on the evolution of the genus. Plant J 93:1088–1101Google Scholar
  75. Li Z, Bi YF, Wang X, Wang YZ, Yang SQ, Zhang ZT, Chen JF, Lou QF (2018b) Chromosome identification in Cucumis anguria revealed by cross-species single-copy gene FISH. Genome 61:397–404Google Scholar
  76. Lin L, Koo DH, Zhang WL, St Peter J, Jiang JM (2011) De novo assembly of potential linear artificial chromosome constructs capped with expansive telomeric repeats. Plant Methods 7:10Google Scholar
  77. Lou QF, Iovene M, Spooner DM, Buell CR, Jiang JM (2010) Evolution of chromosome 6 of Solanum species revealed by comparative fluorescence in situ hybridization mapping. Chromosoma 119:435–442Google Scholar
  78. Lou QF, Zhang YX, He YH, Li J, Jia L, Cheng CY, Guan W, Yang SQ, Chen JF (2014) Single-copy gene-based chromosome painting in cucumber and its application for chromosome rearrangement analysis in Cucumis. Plant J 78:169–179Google Scholar
  79. Lough AN, Faries KM, Koo DH, Hussain A, Roark LM, Langewisch TL, Backes T, Kremling KAG, Jiang JM, Birchler JA, Newton KJ (2015) Cytogenetic and sequence analyses of mitochondrial DNA insertions in nuclear chromosomes of maize. G3 5:2229–2239Google Scholar
  80. Lubeck E, Cai L (2012) Single-cell systems biology by super-resolution imaging and combinatorial labeling. Nat Methods 9:743–748Google Scholar
  81. Lysak MA, Fransz PF, Ali HBM, Schubert I (2001) Chromosome painting in Arabidopsis thaliana. Plant J 28:689–697Google Scholar
  82. Lysak MA, Koch MA, Pecinka A, Schubert I (2005) Chromosome triplication found across the tribe Brassiceae. Genome Res 15:516–525Google Scholar
  83. Lysak MA, Berr A, Pecinka A, Schmidt R, McBreen K, Schubert I (2006) Mechanisms of chromosome number reduction in Arabidopsis thaliana and related Brassicaceae species. Proc Natl Acad Sci U S A 103:5224–5229Google Scholar
  84. Macas J, Kejnovsky E, Neumann P, Novak P, Koblizkova A, Vyskot B (2011) Next generation sequencing-based analysis of repetitive DNA in the model dioecious plant Silene latifolia. PLoS One 6:e27335Google Scholar
  85. Marques A, Ribeiro T, Neumann P, Macas J, Novak P, Schubert V, Pellino M, Fuchs J, Ma W, Kuhlmann M, Brandt R, Vanzela ALL, Beseda T, Simkova H, Pedrosa-Harand A, Houben A (2015) Holocentromeres in Rhynchospora are associated with genome-wide centromere-specific repeat arrays interspersed among euchromatin. Proc Natl Acad Sci U S A 112:13633–13638Google Scholar
  86. Meng Z, Zhang ZL, Yan TY, Lin QF, Wang Y, Huang WY, Huang YJ, Li ZJ, Yu QY, Wang JP, Wang K (2018) Comprehensively characterizing the cytological features of Saccharum spontaneum by the development of a complete set of chromosome-specific oligo probes. Front Plant Sci 9:1624Google Scholar
  87. Nagaki K, Tanaka K, Yamaji N, Kobayashi H, Murata M (2015) Sunflower centromeres consist of a centromere-specific LINE and a chromosome-specific tandem repeat. Front Plant Sci 6:912Google Scholar
  88. Nani TF, Schnable JC, Washburn JD, Albert P, Pereira WA, Sobrinho FS, Birchler JA, Techio VH (2018) Location of low copy genes in chromosomes of Brachiaria spp. Mol Biol Rep 45:109–118Google Scholar
  89. Neumann P, Navratilova A, Schroeder-Reiter E, Koblizkova A, Steinbauerova V, Chocholova E, Novak P, Wanner G, Macas J (2012) Stretching the rules: monocentric chromosomes with multiple centromere domains. PLoS Genet 8:e1002777Google Scholar
  90. Ngo TD, Malone JM, Boutsalis P, Gill G, Preston C (2018) EPSPS gene amplification conferring resistance to glyphosate in windmill grass (Chloris truncata) in Australia. Pest Manag Sci 74:1101–1108Google Scholar
  91. Novak P, Neumann P, Macas J (2010) Graph-based clustering and characterization of repetitive sequences in next-generation sequencing data. BMC Bioinformatics 11:378Google Scholar
  92. Novak P, Neumann P, Pech J, Steinhaisl J, Macas J (2013) RepeatExplorer: a galaxy-based web server for genome-wide characterization of eukaryotic repetitive elements from next-generation sequence reads. Bioinformatics 29:792–793Google Scholar
  93. Paterson AH, Bowers JE, Burow MD, Draye X, Elsik CG, Jiang CX, Katsar CS, Lan TH, Lin YR, Ming RG, Wright RJ (2000) Comparative genomics of plant chromosomes. Plant Cell 12:1523–1539Google Scholar
  94. Pedersen C, Langridge P (1997) Identification of the entire chromosome complement of bread wheat by two-colour FISH. Genome 40:589–593Google Scholar
  95. Pedersen C, Rasmussen SK, LindeLaursen I (1996) Genome and chromosome identification in cultivated barley and related species of the Triticeae (Poaceae) by in situ hybridization with the GAA-satellite sequence. Genome 39:93–104Google Scholar
  96. Perumal S, Waminal NE, Lee J, Lee J, Choi BS, Kim HH, Grandbastien MA, Yang TJ (2017) Elucidating the major hidden genomic components of the A, C, and AC genomes and their influence on Brassica evolution. Sci Rep 7:17986Google Scholar
  97. Powles SB (2010) Gene amplification delivers glyphosate-resistant weed evolution. Proc Natl Acad Sci U S A 107:955–956Google Scholar
  98. Puterova J, Razumova O, Martinek T, Alexandrov O, Divashuk M, Kubat Z, Hobza R, Karlov G, Kejnovsky E (2017) Satellite DNA and transposable elements in seabuckthorn (Hippophae rhamnoides), a dioecious plant with small Y and large X chromosomes. Genome Biol Evol 9:197–212Google Scholar
  99. Qu MM, Li KP, Han YL, Chen L, Li ZY, Han YH (2017) Integrated karyotyping of woodland strawberry (Fragaria vesca) with oligopaint FISH probes. Cytogenet Genome Res 153:158–164Google Scholar
  100. Ribeiro T, Marques A, Novak P, Schubert V, Vanzela ALL, Macas J, Houben A, Pedrosa-Harand A (2017) Centromeric and non-centromeric satellite DNA organisation differs in holocentric Rhynchospora species. Chromosoma 126:325–335Google Scholar
  101. Robledillo LA, Koblizkova A, Novak P, Bottinger K, Vrbova I, Neumann P, Schubert I, Macas J (2018) Satellite DNA in Vicia faba is characterized by remarkable diversity in its sequence composition, association with centromeres, and replication timing. Sci Rep 8:5838Google Scholar
  102. Ruban AS, Badaeva ED (2018) Evolution of the S-genomes in Triticum-Aegilops alliance: evidences from chromosome analysis. Front Plant Sci 9:1756Google Scholar
  103. Ruiz-Ruano FJ, Lopez-Leon MD, Cabrero J, Camacho JPM (2016) High-throughput analysis of the satellitome illuminates satellite DNA evolution. Sci Rep 6:28333Google Scholar
  104. Said M, Hribova E, Danilova TV, Karafiatova M, Cizkova J, Friebe B, Dolezel J, Gill BS, Vrana J (2018) The Agropyron cristatum karyotype, chromosome structure and cross-genome homoeology as revealed by fluorescence in situ hybridization with tandem repeats and wheat single-gene probes. Theor Appl Genet 131:2213–2227Google Scholar
  105. Salas RA, Dayan FE, Pan ZQ, Watson SB, Dickson JW, Scott RC, Burgos NR (2012) EPSPS gene amplification in glyphosate-resistant Italian ryegrass (Lolium perenne ssp multiflorum) from Arkansas. Pest Manag Sci 68:1223–1230Google Scholar
  106. Schmidt T, HeslopHarrison JS (1996) The physical and genomic organization of microsatellites in sugar beet. Proc Natl Acad Sci U S A 93:8761–8765Google Scholar
  107. Schubert I, Fransz PF, Fuchs J, de Jong JH (2001) Chromosome painting in plants. Methods Cell Sci 23:57–69Google Scholar
  108. Schwarzacher T, Leitch AR, Bennett MD, Heslopharrison JS (1989) In situ localization of parental genomes in a wide hybrid. Ann Bot (London) 64:315–324Google Scholar
  109. Setiawan AB, Teo CH, Kikuchi S, Sassa H, Koba T (2018) An improved method for inducing prometaphase chromosomes in plants. Mol Cytogenet 11:32Google Scholar
  110. Sharma S, Raina SN (2005) Organization and evolution of highly repeated satellite DNA sequences in plant chromosomes. Cytogenet Genome Res 109:15–26Google Scholar
  111. Stupar RM, Lilly JW, Town CD, Cheng Z, Kaul S, Buell CR, Jiang JM (2001) Complex mtDNA constitutes an approximate 620-kb insertion on Arabidopsis thaliana chromosome 2: implication of potential sequencing errors caused by large-unit repeats. Proc Natl Acad Sci U S A 98:5099–5103Google Scholar
  112. Szinay D, Wijnker E, van den Berg R, Visser RGF, de Jong H, Bai YL (2012) Chromosome evolution in Solanum traced by cross-species BAC-FISH. New Phytol 195:688–698Google Scholar
  113. Tang XM, Szinay D, Lang C, Ramanna MS, van der Vossen EAG, Datema E, Lankhorst RK, de Boer J, Peters SA, Bachem C, Stiekema W, Visser RGF, de Jong H, Bai YL (2008) Crosss species bacterial artificial chromosome-fluorescence in situ hybridization painting of the tomato and potato chromosome 6 reveals undescribed chromosomal rearrangements. Genetics 180:1319–1328Google Scholar
  114. Tang ZX, Yang ZJ, Fu SL (2014) Oligonucleotides replacing the roles of repetitive sequences pAs1, pSc119.2, pTa-535, pTa71, CCS1, and pAWRC.1 for FISH analysis. J Appl Genet 55:313–318Google Scholar
  115. Tang SY, Qiu L, Xiao ZQ, Fu SL, Tang ZX (2016) New oligonucleotide probes for ND-FISH analysis to identify barley chromosomes and to investigate polymorphisms of wheat chromosomes. Genes-Basel 7:118Google Scholar
  116. Tiwari VK, Wang SC, Danilova T, Koo DH, Vrana J, Kubalakova M, Hribova E, Rawat N, Kalia B, Singh N, Friebe B, Dolezel J, Akhunov E, Poland J, Sabir JSM, Gill BS (2015) Exploring the tertiary gene pool of bread wheat: sequence assembly and analysis of chromosome 5M(g) of Aegilops geniculata. Plant J 84:733–746Google Scholar
  117. Torres GA, Gong ZY, Iovene M, Hirsch CD, Buell CR, Bryan GJ, Novak P, Macas J, Jiang JM (2011) Organization and evolution of subtelomeric satellite repeats in the potato genome. G3 1:85–92Google Scholar
  118. Vasconcelos EV, Fonseca AFD, Pedrosa-Harand A, Bortoleti KCD, Benko-Iseppon AM, da Costa AF, Brasileiro-Vidal AC (2015) Intra- and interchromosomal rearrangements between cowpea [Vigna unguiculata (L.) Walp.] and common bean (Phaseolus vulgaris L.) revealed by BAC-FISH. Chromosom Res 23:253–266Google Scholar
  119. Waminal NE, Pellerin RJ, Kim NS, Jayakodi M, Park JY, Yang TJ, Kim HH (2018) Rapid and efficient FISH using pre-labeled oligomer probes. Sci Rep 8:8224Google Scholar
  120. Xin H, Zhang T, Han Y, Wu Y, Shi J, Xi M, Jiang JM (2018) Chromosome painting and comparative physical mapping of the sex chromosomes in Populus tomentosa and Populus deltoides. Chromosoma 127:313–321Google Scholar
  121. Yamada NA, Rector LS, Tsang P, Carr E, Scheffer A, Sederberg MC, Aston ME, Ach RA, Tsalenko A, Sampas N, Peter B, Bruhn L, Brothman AR (2011) Visualization of fine-scale genomic structure by oligonucleotide-based high-resolution FISH. Cytogenet Genome Res 132:248–254Google Scholar
  122. Yan HH, Talbert PB, Lee HR, Jett J, Henikoff S, Chen F, Jiang JM (2008) Intergenic locations of rice centromeric chromatin. PLoS Biol 6:2563–2575Google Scholar
  123. Yang SQ, Qin XD, Cheng CY, Li Z, Lou QF, Li J, Chen JF (2017) Organization and evolution of four differentially amplified tandem repeats in the Cucumis hystrix genome. Planta 246:749–761Google Scholar
  124. Yang XM, Zhao HN, Zhang T, Zeng ZX, Zhang PD, Zhu B, Han YH, Braz GT, Casler MD, Schmutz J, Jiang JM (2018) Amplification and adaptation of centromeric repeats in polyploid switchgrass species. New Phytol 218:1645–1657Google Scholar
  125. Yu WC, Lamb JC, Han FP, Birchler JA (2007) Cytological visualization of DNA transposons and their transposition pattern in somatic cells of maize. Genetics 175:31–39Google Scholar
  126. Zhang P, Li WL, Fellers J, Friebe B, Gill BS (2004) BAC-FISH in wheat identifies chromosome landmarks consisting of different types of transposable elements. Chromosoma 112:288–299Google Scholar
  127. Zhang HQ, Koblizkova A, Wang K, Gong ZY, Oliveira L, Torres GA, Wu YF, Zhang WL, Novak P, Buell CR, Macas J, Jiang JM (2014) Boom-bust turnovers of megabase-sized centromeric DNA in Solanum species: rapid evolution of DNA sequences associated with centromeres. Plant Cell 26:1436–1447Google Scholar
  128. Zhang C, Feng L, He TT, Yang CH, Chen GQ, Tian XS (2015) Investigating the mechanisms of glyphosate resistance in goosegrass (Eleusine indica) population from South China. J Integr Agric 14:909–918Google Scholar
  129. Zhang WP, Zuo S, Li ZJ, Meng Z, Han JL, Song JQ, Pan YB, Wang K (2017) Isolation and characterization of centromeric repetitive DNA sequences in Saccharum spontaneum. Sci Rep 7:41659Google Scholar
  130. Zhao HN, Zeng ZX, Koo DH, Gill BS, Birchler JA, Jiang JM (2017) Recurrent establishment of de novo centromeres in the pericentromeric region of maize chromosome 3. Chromosom Res 25:299–311Google Scholar
  131. Zheng JS, Sun CZ, Zhang SN, Hou XL, Bonnema G (2016) Cytogenetic diversity of simple sequences repeats in morphotypes of Brassica rapa ssp chinensis. Front Plant Sci 7:1049Google Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Department of Plant Biology, Department of HorticultureMichigan State UniversityEast LansingUSA

Personalised recommendations